Abstract
The complete mitochondrial genome provides crucial information for comprehending gene rearrangement, molecular evolution, and phylogenetic analysis. Here, we have determined the complete mitogenome sequence of Gonatopsis borealis and Onychoteuthis compacta for the first time. Their genome sizes were 20,148 bp and 20,491 bp, respectively, including 18 protein-coding genes, COI-COIII, ATP6, and ATP8 are duplicated, 23 transfer RNA genes, and 2 ribosomal RNA (rRNA) genes (12S and 16S rRNA). Specifically, the overall A+T content is 70.69% and 72.67%. It shows a significant AT bias. The whole mitogenomes indicate positive AT skew (0.070 and 0.062). Furthermore, the gene order has been rearranged within Oegopsida. The tandem duplication random loss model was determined as most likely to explain the observed gene rearrangements. Phylogenetic analysis was performed, and the result tree was found to be consistent with the morphological identification classification. Estimation of divergence time for 35 species showed that the main differentiation of Oegopsida occurred in 140.70 Mya. These results will help to better understand the gene rearrangements and evolution of G. borealis and O. compacta and lay a foundation for further phylogeny genetic studies of Oegopsida.
Similar content being viewed by others
References
Akasaki T, Nikaido M, Tsuchiya K, Segawa S, Hasegawa M, Okada N (2006) Extensive mitochondrial gene arrangements in coleoid Cephalopoda and their phylogenetic implications. Mol Phylogenet Evol 3:648–658. https://doi.org/10.1016/j.ympev.2005.10.018
Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25(22):4692–3. https://doi.org/10.1093/nar/25.22.4692
Allcock AL, Cooke IR (2011) What can the mitochondrial genome reveal about higher-level phylogeny of the molluscan class Cephalopoda? Zool J Linn Soc 161(3):573–586. https://doi.org/10.1111/j.1096-3642.2010.00656.x
Anderson FE, Lindgren AR (2021) Phylogenomic analyses recover a clade of large-bodied decapodiform cephalopods. Mol Phylogenet Evol. https://doi.org/10.1016/j.ympev.2020.107038
Bernt M, Bleidorn C, Braband A, Dambach J, Donath A, Fritzsch G, Golombek A, Hadrys H, Jühling F, Meusemann K, Middendorf M, Misof B, Perseke M, Podsiadlowski L, von Reumont B, Schierwater B, Schlegel M, Schrödl M, Simon S, Stadler PF, Stöger I, Struck TH (2013) A comprehensive analysis of bilaterian mitochondrial genomes and phylogeny. Mol Phylogenet Evol 2:352–364. https://doi.org/10.1016/j.ympev.2013.05.002
Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol 2:313–319. https://doi.org/10.1016/j.ympev.2012.08.023
Bolstad KSR, Braid HE, Strugnell JM, Lindgren AR, Lischka A, Kubodera T, Laptikhovsky VL, Roura Labiaga A (2018) A mitochondrial phylogeny of the family Onychoteuthidae (Cephalopoda: Oegopsida). Mol Phylogenet Evol. https://doi.org/10.1016/j.ympev.2018.05.032
Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 4:e1003537. https://doi.org/10.1371/journal.pcbi.1003537
Cummings MP (2014) PAUP* (Phylogenetic Analysis Using Parsimony (and Other Methods)) Dictionary of Bioinformatics and Computational Biology
Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T (2020) ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol Biol Evol 1:291–294. https://doi.org/10.1093/molbev/msz189
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3(5):294–299
Guo B, Chen Y, Zhang C, Lv Z, Xu KA, Ping H, Shi H (2018) Characterization of complete mitochondrial genome and phylogeny of Sepia lycidas (Sepioidea, Sepiidae). Pak J Zool. https://doi.org/10.17582/journal.pjz/2018.50.4.1497.1508
Hamasaki K, Iizuka C, Sanda T, Imai H, Kitada S (2017) Phylogeny and phylogeography of the land hermit crab Coenobita purpureus (Decapoda: Anomura: Coenobitidae) in the Northwestern Pacific Region. Mar Ecol 1:e12369. https://doi.org/10.1111/maec.12369
Hendrickx ME, Urbano B, Zamorano P (2015) Distribution of pelagic squids Abraliopsis Joubin, 1896 (Enoploteuthidae) and Pterygioteuthis P. Fischer, 1896 (Pyroteuthidae) (Cephalopoda, Decapodiformes, Oegopsida) in the Mexican Pacific. ZooKeys 537:51–64. https://doi.org/10.3897/zookeys.537.6023
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 6:587–589. https://doi.org/10.1038/nmeth.4285
Katugin ON, Chichvarkhina OV, Zolotova AO, Chichvarkhin AY (2017) DNA barcoding for squids of the family Gonatidae (Cephalopoda: Teuthida) from the boreal North Pacific. Mitochondrial DNA Part A 1:41–49. https://doi.org/10.3109/19401736.2015.1110792
Kawashima Y, Nishihara H, Akasaki T, Nikaido M, Tsuchiya K, Segawa S, Okada N (2013) The complete mitochondrial genomes of deep-sea squid (Bathyteuthis abyssicola), bob-tail squid (Semirossia patagonica) and four giant cuttlefish (Sepia apama, S. latimanus, S. lycidas and S. pharaonis), and their application to the phylogenetic analysis of Decapodiformes. Mol Phylogenet Evol 69(3):980–93. https://doi.org/10.1016/j.ympev.2013.06.007
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 7:1870–1874. https://doi.org/10.1093/molbev/msw054
Letunic I, Bork P (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics (Oxford, England) 1:127–128. https://doi.org/10.1093/bioinformatics/btl529
Lindgren AR (2010) Molecular inference of phylogenetic relationships among Decapodiformes (Mollusca: Cephalopoda) with special focus on the squid order Oegopsida. Mol Phylogenet Evol 1:77–90. https://doi.org/10.1016/j.ympev.2010.03.025
Lindgren AR, Daly M (2007) The impact of length-variable data and alignment criterion on the phylogeny of Decapodiformes (Mollusca: Cephalopoda). Cladistics 23(5):464–476
Lindgren AR, Giribet G, Nishiguchi MK (2004) A combined approach to the phylogeny of Cephalopoda (Mollusca). Cladistics 5:454–486. https://doi.org/10.1111/j.1096-0031.2004.00032.x
Lindgren AR, Pankey MS, Hochberg FG, Oakley TH (2012) A multi-gene phylogeny of Cephalopoda supports convergent morphological evolution in association with multiple habitat shifts in the marine environment. BMC Evol Biol 12:129. https://doi.org/10.1186/1471-2148-12-129
Miao J, Feng J, Liu X, Yan C, Ye Y, Li J, Xu K, Guo B, Lü Z (2022) Sequence comparison of the mitochondrial genomes of five brackish water species of the family Neritidae: phylogenetic implications and divergence time estimation. Ecol Evol 6:e8984. https://doi.org/10.1002/ece3.8984
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 1:268–274. https://doi.org/10.1093/molbev/msu300
Pardo-Gandarillas MC, Torres FI, Fuchs D, Ibáñez CM (2018) Updated molecular phylogeny of the squid family Ommastrephidae: Insights into the evolution of spawning strategies. Mol Phylogenet Evol 120:212–217. https://doi.org/10.1016/j.ympev.2017.12.014
Perna NT, Kocher TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J Mol Evol 41:353–358
Rambaut AJC (2017) http://tree.bio.ed.ac.uk/software/figtree. FigTree-version 1.4. 3, a graphical viewer of phylogenetic trees
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 3:539–542. https://doi.org/10.1093/sysbio/sys029
Roper CF, Young RE, Voss GL (1969) An illustrated key to the families of the order Teuthoidea (Cephalopoda). Smithson Contrib Zool. https://doi.org/10.5479/si.00810282.13
Rozas J, Rozas R (1995) DnaSP, DNA sequence polymorphism: an interactive program for estimating population genetics parameters from DNA sequence data. Comput Appl Biosci 6:621–625. https://doi.org/10.1093/bioinformatics/11.6.621
Sanchez G, Setiamarga DHE, Tuanapaya S, Tongtherm K, Winkelmann IE, Schmidbaur H, Umino T, Albertin C, Allcock L, Perales-Raya C, Gleadall I, Strugnell JM, Simakov O, Nabhitabhata J (2018) Genus-level phylogeny of cephalopods using molecular markers: current status and problematic areas. PeerJ 6:e4331. https://doi.org/10.7717/peerj.4331
Stothard P, Wishart DS (2005) Circular genome visualization and exploration using CGView. Bioinformatics (Oxford, England) 4:537–539. https://doi.org/10.1093/bioinformatics/bti054
Strugnell J, Nishiguchi MK (2007) Molecular phylogeny of coleoid cephalopods (Mollusca: Cephalopoda) inferred from three mitochondrial and six nuclear loci: a comparison of alignment, implied alignment and analysis methods. J Molluscan Stud 4:399–410. https://doi.org/10.1093/mollus/eym038
Tang Y, Zhang X, Ma Y, Zheng X (2021) Descriptive study of the mitogenome of the diamondback squid (Thysanoteuthis rhombus Troschel, 1857) and the evolution of mitogenome arrangement in oceanic squids. J Zool Syst Evol Res 5:981–991. https://doi.org/10.1111/jzs.12478
Uribe JE, Zardoya R (2017) Revisiting the phylogeny of Cephalopoda using complete mitochondrial genomes. J Molluscan Stud 83(2):133–144
Wakabayashi T, Suzuki N, Sakai M, Ichii T, Chow S (2012) Phylogenetic relationships among the family Ommastrephidae (Mollusca: Cephalopoda) inferred from two mitochondrial DNA gene sequences. Marine Genomics. https://doi.org/10.1016/j.margen.2012.04.005
Xia X (2013) DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution. Mol Biol Evol 7:1720–1728. https://doi.org/10.1093/molbev/mst064
Yokobori S, Fukuda N, Nakamura M, Aoyama T, Oshima T (2004) Long-term conservation of six duplicated structural genes in cephalopod mitochondrial genomes. Mol Biol Evol 11:2034–2046. https://doi.org/10.1093/molbev/msh227
Yokobori SI, Lindsay DJ, Yoshida M, Tsuchiya K, Oshima TJMP (2007) Mitochondrial genome structure and evolution in the living fossil vampire squid Vampyroteuthis infernalis, and extant cephalopods. Mol Phylogenet Evol 44(2):898–910
Young RE, Vecchione M, Donovan DT (1998) The evolution of coleoid cephalopods and their present biodiversity and ecology. S Afr J Marine Sci 1:393–420. https://doi.org/10.2989/025776198784126287
Acknowledgements
This work was supported by Program on the Survey, Monitoring and Assessment of Global Fishery Resources (Comprehensive scientific survey of fisheries resources at the high seas) sponsored by the Ministry of Agriculture and Rural Affairs; Zhejiang Provincial Natural Science Foundation of China (Grant No. LY20C190008).
Funding
Funding was provided by Zhejiang Provincial Natural Science Foundation of China (Grant No. LY20C190008), Program on the Survey, Monitoring and Assessment of Global Fishery Resources (Comprehensive scientific survey of fisheries resources at the high seas) sponsored by the Ministry of Agriculture and Rural Affairs.
Author information
Authors and Affiliations
Contributions
LJ conceived this research and designed the experiment. FF and LP performed experiments. FF, LJ, LP, YY, YFL, BL analyzed data. FF and LJ wrote the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Competing Interests
The authors have not disclosed any competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Fan, F., Pei, L., Jiang, L. et al. Gene Rearrangements in the Mitochondrial Genome of Gonatopsis borealis and Onychoteuthis compacta Reveal Their Phylogenetic Implications for Oegopsida. Biochem Genet (2024). https://doi.org/10.1007/s10528-024-10707-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10528-024-10707-7